Incomplete lineage sorting and ancient admixture, and speciation without morphological change in ghost-worm cryptic species.

José Cerca,Julian M Catchen,Mark Ravinet,Michael D Nowak,Mafalda S Ferreira,Angel G Rivera-Colón,Torsten H Struck

doi:10.7717/peerj.10896

Abstract

Morphologically similar species, that is cryptic species, may be similar or quasi-similar owing to the deceleration of morphological evolution and stasis. While the factors underlying the deceleration of morphological evolution or stasis in cryptic species remain unknown, decades of research in the field of paleontology on punctuated equilibrium have originated clear hypotheses. Species are expected to remain morphologically identical in scenarios of shared genetic variation, such as hybridization and incomplete lineage sorting, or in scenarios where bottlenecks reduce genetic variation and constrain the evolution of morphology. Here, focusing on three morphologically similar Stygocapitella species, we employ a whole-genome amplification method (WGA) coupled with double-digestion restriction-site associated DNA sequencing (ddRAD) to reconstruct the evolutionary history of the species complex. We explore population structure, use population-level statistics to determine the degree of connectivity between populations and species, and determine the most likely demographic scenarios which generally reject for recent hybridization. We find that the combination of WGA and ddRAD allowed us to obtain genomic-level data from microscopic eukaryotes (∼1 millimetre) opening up opportunities for those working with population genomics and phylogenomics in such taxa. The three species share genetic variance, likely from incomplete lineage sorting and ancient admixture. We speculate that the degree of shared variation might underlie morphological similarity in the Atlantic species complex.

Highlights

The characterization and delimitation of species and populations using DNA sequencing and barcoding has led to the discovery of ‘hidden species diversity’ in previously established species (Knowlton, 1993; Bickford et al, 2007; Pfenninger & Schwenk, 2007; Struck et al, 2018)
When species are poorly delimited, determination of biogeographic breaks (Weber, Stöhr & Chenuil, 2019; Cerca et al, 2020a), inferences on the evolutionary history (Wada, Kameda & Chiba, 2013; Swift, Daglio & Dawson, 2016; Struck et al, 2018; Dufresnes et al, 2019), and the determination of ecological richness of an ecosystem (Chenuil et al, 2019) may be severely compromised. These problems extend outside fundamental fields of biology when species complexes are medically-relevant, such as the Anopheles cryptic species complex where not every morphologically-similar species is capable of transmitting malaria (Erlank, Koekemoer & Coetzee, 2018) or in parasite species (De León & Nadler, 2010; Nadler & De Len, 2011), and in cases of conservation management (Bickford et al, 2007; Bernardo, 2011)
While our sampling design does not account for genetic constraints, we study the evolutionary history of Stygocapitella species seeking to determine signals of loss of genetic variation or shared

Summary

Introduction

The characterization and delimitation of species and populations using DNA sequencing and barcoding has led to the discovery of ‘hidden species diversity’ in previously established species (Knowlton, 1993; Bickford et al, 2007; Pfenninger & Schwenk, 2007; Struck et al, 2018). On the one other side, the ‘‘evolutionary framework’’ suggests that the deceleration of morphological evolution is a plausible expectation, given the observation of stasis, niche conservatism and constraints in nature While some of this diversity is potentially attributed to taxonomic artefacts (Korshunova et al, 2017), morphologically similar species—‘true’ cryptic species—have been discovered in various branches of the tree of life, representing an important part of biodiversity (Pfenninger & Schwenk, 2007; Pérez-Ponce de León & Poulin, 2016; Cerca, Purschke & Struck, 2018; Fišer, Robinson & Malard, 2018). These problems extend outside fundamental fields of biology when species complexes are medically-relevant, such as the Anopheles cryptic species complex where not every morphologically-similar species is capable of transmitting malaria (Erlank, Koekemoer & Coetzee, 2018) or in parasite species (De León & Nadler, 2010; Nadler & De Len, 2011), and in cases of conservation management (Bickford et al, 2007; Bernardo, 2011)

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Conclusion